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Cladogenesis and Reticulation in Cuscuta Sect. Denticulatae (Convolvulaceae)

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Cladogenesis and Reticulation in Cuscuta Sect. Denticulatae (Convolvulaceae) Organisms Diversity & Evolution (2018) 18:383–398 https://doi.org/10.1007/s13127-018-0383-5 ORIGINAL ARTICLE Cladogenesis and reticulation in Cuscuta sect. Denticulatae (Convolvulaceae) Miguel A. García1,2 & SašaStefanović1 & Catherine Weiner3 & Magdalena Olszewski3 & Mihai Costea3 Received: 5 May 2018 /Accepted: 11 October 2018 /Published online: 28 October 2018 # The Author(s) 2018 Abstract As traditionally circumscribed, Cuscuta sect. Denticulatae is a group of three parasitic plant species native to the deserts of Western USA (Cuscuta denticulata, Cuscuta nevadensis) and the central region of Baja California, Mexico (Cuscuta veatchii). Molecular phylogenetic studies confirmed the monophyly of this group and suggested that the disjunct C. veatchii is a hybrid between the other two species. However, the limited sampling left the possibility of alternative biological and methodological explanations. We expanded our sampling to multiple individuals of all the species collected from across their entire geographical ranges. Sequence data from the nuclear and plastid regions were used to reconstruct the phylogeny and find out if the topological conflict was maintained. We obtained karyotype information from multiple individuals, investigated the morphological variation of the group thorough morphometric analyses, and compiled data on ecology, host range, and geographical distribution. Our results confirmed that C. veatchii is an allotetraploid. Furthermore, we found previously unknown autotetraploid population of C. denticulata, and we describe a new hybrid species, Cuscuta psorothamnensis. We suggest that this newly discovered natural hybrid is resulting from an independent (and probably more recent) hybridization event between the same diploid parental species as those of C. veatchii. All the polyploids showed host shift associated with hybridization and/or polyploidy and are found growing on hosts that are rarely or never frequented by their diploid progenitors. The great potential of this group as a model to study host shift in parasitic plants associated with recurrent allopolyploidy is discussed. Keywords Host shift . Host range . Hybridization . Polyploidy . Parasitic plant . Speciation Introduction cosmopolitan but the majority of species are native to North and South America, belonging to Cuscuta subg. Grammica,the Cuscuta (dodders) is a plant genus of nearly 200 species of largest infrageneric group that includes more than 150 species stem parasites (Yuncker 1932;Garcíaetal.2014; Costea et al. (Costea et al. 2015a). Dodders occur in a great variety of hab- 2015a) that has evolved within Convolvulaceae (reviewed by itats, from temperate to tropical, desert to riparian, littoral to Stefanović and Olmstead 2004, 2005). The genus is nearly high mountains, grasslands, forests, saline, and disturbed hab- itats. Similarly to other parasitic plants, dodders act as keystone species in their ecosystems (Press and Phoenix 2005;Graffis Miguel A. García and Saša Stefanović contributed equally to this work. and Kneitel 2015). Approximately 15–20 Cuscuta spp. world- Electronic supplementary material The online version of this article wide are agricultural and horticultural pests (Dawson et al. (https://doi.org/10.1007/s13127-018-0383-5) contains supplementary 1994; Costea and Tardif 2006), and in most countries, control material, which is available to authorized users. and quarantine measures target the genus as a whole, ignoring * Miguel A. García the fact that some species may be endangered or even threat- [email protected] ened with extinction (Costea and Stefanović 2009). Stefanović et al. (2007) noted several cases of conflict be- tween plastid- and nuclear-derived phylogenies indicative of 1 Department of Biology, University of Toronto Mississauga, Mississauga, ON L5L 1C6, Canada possible reticulation in Cuscuta subg. Grammica.Tofurther investigate the origin of these conflicts, Stefanović and Costea 2 Royal Botanic Gardens Kew, Richmond, Surrey TW9 3AE, UK 3 (2008)expandedtheirtrnL-F and nrITS matrices through ad- Department of Biology, Wilfrid Laurier University, dition of multiple sequences from 105 species from this Waterloo, ON N2L3C5, Canada 384 García M.A. et al. subgenus and found five cases of species with a probable hybrid origin. A series of statistical tests by Stefanović and Costea (2008) showed that alternative hypotheses to explain discordant gene topologies, such as incomplete lineage sorting, undetected paralogy, or horizontal gene transfer, were not supported. All these cases in subg. Grammica were con- firmed and three additional ones were detected using rbcL and nrLSU sequences in a broader phylogenetic context with rep- resentatives of the entire genus (García et al. 2014). Several cases of topological incongruence were also found for Cuscuta subg. Cuscuta by García and Martín (2007), but the origin of the conflicts was not further investigated. Costea and Stefanović (2010) discovered that at least four independent hybridization events had occurred in the evolution of Cuscuta sect. Umbellatae (subg. Grammica), two more for this section than previously detected. More recently, a detailed study by Costea et al. (2015b)onCuscuta sect. Cleistogrammica (subg. Grammica) showed that the worldwide invasive weed Cuscuta campestris Yunck (1932) has two divergent groups of nrITS ribotypes. Both of these disparate ribotypes are topologi- cally incongruent with the plastid trnL-F phylogeny, in aggregate suggesting the hybrid origin of C. campestris (Costea et al. 2015b). Another striking case of topological discordance was found within Cuscuta sect. Denticulatae (Stefanović and Costea 2008;Garcíaetal.2014). This group of species in subg. Grammica is well characterized morphologically by the radic- ular end of the embryo spherically enlarged in a ball-like structure that increases in volume during seed maturation (Costea et al. 2015a). Such a feature is not present in any other clade of Cuscuta and this synapomorphy is thought to be an adaptation for seed germination on the host while the fruit is still enclosed by the perianth (vivipary). The enlarged embryo probably stores nutrients and water as an adaptation to germi- nation in desert environments (Costea et al. 2005). Section Denticulatae includes three species distributed in Fig. 1 Distribution of Cuscuta sect. Denticulatae species across their Western USA (Cuscuta denticulata Engelm.; Cuscuta geographic ranges in western North America. Potential extent of nevadensis I.M.Johnst.) and the Central Desert of Baja distribution for C. denticulata is outlined and that of C. nevadensis is shaded. Approximate positions of sampling sites used in this study are California in Mexico (Cuscuta veatchii Brandegee) (Fig. 1). indicated (for details, see Appendix 1). Circles (solid and open) represent Of the three species, C. denticulata has the broadest geograph- sampling sites for populations of C. denticulata, squares (solid and open) ical distribution and host preference, whereas C. nevadensis represent those of C. nevadensis, triangles those of C. veatchii, while X has narrower geographical and host ranges, occurring sympat- symbols stand for the newly described species, C. psorothamnensis. Encircled symbols represent material obtained from herbaria; all others rically with C. denticulata (Costea et al. 2005). Cuscuta are sampled directly in the field, including multiple individuals per pop- veatchii has a disjunct distribution and grows only on ulation. Solid and open symbols correspond to different haplo- and Pachycormus discolor (Benth.) Coville (Anacardiaceae). ribotypes of C. denticulata and C. nevadensis (see text for details) The phylogenetic analyses by Stefanović and Costea (2008) placed C. veatchii in a clade with C. denticulata on the nrITS tree, whereas this species was resolved with C. nevadensis on to find statistical difference between optimal and constrained the plastid trnL-F tree, in both cases with 100% bootstrap trees among plastid and nuclear data. Also, in that study, the support. The authors concluded that this topological incongru- sampling was limited to two to three individuals per species, ence, together with the life history, ecological, and biogeo- and because the clade included only three taxa and a root, a graphical data, was consistent with a hybrid origin of topological distortion such a nearest-neighbor interchange C. veatchii. However, some alternative topology tests failed (NNI) could not be ruled out, leaving ancestral polymorphism Cladogenesis and reticulation in Cuscuta sect. Denticulatae (Convolvulaceae) 385 or incomplete lineage sorting as viable alternative explana- population sequence variation of DNA markers, two to five tions for the discordance between nuclear and plastid trees. individuals were sampled per locality in our field trips. Within In the present study, we further investigate the hybridiza- a locality, multiple specimens were collected growing on sep- tion hypothesis for the origin of C. veatchii by expanding our arate host plants (> 1 m apart from each other). Despite the sampling to multiple individuals for all species involved from host separation, some of the specimens still could be a product their entire geographical distribution as well as by obtaining of multiple individual seedlings infecting a plant (Costea and additional critically needed corroborating information. Thus, Tardif 2006), and we considered these to be Bbulked^ individ- the objectives of this study are (1) to analyze new nrITS and uals.
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